Glioblastoma: A pathogenic crosstalk between tumor cells and pericytes

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Caspani, Elisabetta M ^a   Crossley, Philip H ^a   Redondo Garcia, Carolina ^a   Martinez, Salvador ^a,b  

^a INSTITUTO DE NEUROCIENCIAS   (Spain)

^b Centro de Investigación Biosanitaria en Red de Salud Mental Instituto Murciano de Investigación Biosanitaria Arrixaca   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; LAMININ; PROTEIN CDC42; SILICONE; CD44 PROTEIN, HUMAN; HERMES ANTIGEN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; CANCER GROWTH; CANCER INHIBITION; CANCER SURVIVAL; CELL ACTIVITY; CELL FUNCTION; CELL FUSION; CELL INTERACTION; COCULTURE; CONTROLLED STUDY; CYTOPLASM; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; HYPOXIA; INNATE IMMUNITY; MACROPHAGE; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PERICYTE; PHAGOCYTE; PHENOTYPE; PROTEIN FUNCTION; TUMOR INVASION; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; ANIMAL; BRAIN; BRAIN TUMOR; CANCER STEM CELL; CANCER TRANSPLANTATION; CARCINOGENESIS; CELL SURFACE; CYTOLOGY; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; RNA INTERFERENCE; TRANSGENIC MOUSE; TUMOR CELL LINE; VASCULARIZATION; XENOGRAFT;

ANIMALS; ANTIGENS, CD44; BRAIN; BRAIN NEOPLASMS; CARCINOGENESIS; CDC42 GTP-BINDING PROTEIN; CELL LINE, TUMOR; CELL SURFACE EXTENSIONS; GLIOBLASTOMA; HUMANS; MICE; MICE, NUDE; MICE, TRANSGENIC; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; PERICYTES; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSPLANTATION, HETEROLOGOUS;

EID: 84904512087     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101402     Document Type: Article

References (70)

1. Burger PC, Scheithauer BW (2007) Tumors of the Central Nervous System: AFIP Atlas of Tumor Pathology. Washington DC: American Registry of Pathology Press, Series 4. pp. 65-66.
2. Farin A, Suzuki SO, Weiker M, Goldman JE, Bruce JN, et al. (2006) Transplanted glioma cells migrate and proliferate on host brain vasculature: a dynamic analysis. Glia 53: 799-808.
3. Holash J, Maisonpierre PC, Compton D, Boland P, Alexander CR, et al. (1999) Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 284: 1994-1998. (Pubitemid 29309448)
4. Budde MD, Gold E, Jordan EK, Smith-Brown M, Frank JA (2012) Phase contrast MRI is an early marker of micrometastatic breast cancer development in the rat brain. NMR Biomed 25: 726-736.
5. Bergers G, Hanahan D (2008) Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 8: 592-603.
6. Donnem T, Hu J, Ferguson M, Adighibe O, Snell C, et al. (2013) Vessel cooption in primary human tumors and metastasis: an obstacle to effective antiangiogenic treatment? Cancer Med 2: 427-436.
7. Qian CN (2013) Hijacking the vasculature in ccRCC-co-option, remodelling and angiogenesis. Nat Rev Urol 10: 300-304.
8. Franco M, Pàez-Ribes M, Cortez E, Casanovas O, Pietras K (2011) Use of a mouse model of pancreatic neuroendocrine tumors to find pericyte biomarkers of resistance to anti-angiogenic therapy. Horm Metab Res 43: 884-889.
9. Peppiatt CM, Howarth C, Mobbs P, Attwell D (2006) Bidirectional control of CNS capillary diameter by pericytes. Nature 443: 700-704. (Pubitemid 44564713)
10. Hall CN, Reynell C, Gesslein B, Hamilton NB, Mishra A, et al. (2014) Capillary pericytes regulate cerebral blood flow in health and disease. Nature 508: 55-60.
11. Appaix F, Nissou MF, van der Sanden B, Dreyfus M, Berger F, et al. (2014) Brain mesenchymal stem cells: The other stem cells of the brain? World J Stem Cells 6: 134-143.
12. Dore-Duffy P (2008) Pericytes: pluripotent cells of the blood brain barrier. Curr Pharm Des 14: 1581-1593.
13. Corselli M, Crisan M, Murray IR, West CC, Scholes J, et al. (2013) Identification of perivascular mesenchymal stromal/stem cells by flow cytometry. Cytometry A 83: 714-720.
14. Pieper C, Marek JJ, Unterberg M, Schwerdtle T, Galla HJ (2014) Brain capillary pericytes contribute to the immune defense in response to cytokines or LPS in vitro. Brain Res 1550: 1-8. doi: 10.1016/j.brainres.2014.01.004.
15. Ochs K, Sahm F, Opitz CA, Lanz TV, Oezen I, et al. (2013) Immature mesenchymal stem cell-like pericytes as mediators of immunosuppression in human malignant glioma. J Neuroimmunol 265: 106-116.
16. Thomas WE (1999) Brain macrophages: on the role of pericytes and perivascular cells. Brain Res Brain Res Rev 31: 42-57.
17. Balabanov R, Washington R, Wagnerova J, Dore-Duffy P (1996) CNS microvascular pericytes express macrophage-like function, cell surface integrin alpha M, and macrophage marker ED-2. Microvasc Res 52: 127-142. (Pubitemid 26344909)
18. Hurtado-Alvarado G, Cabañas-Morales AM, Gómez- Gónzalez B (2014) Pericytes: brain-immune interface modulators. Front Integr Neurosci 7: 80. doi: 10.3389/fnint.2013.00080. eCollection 2014.
19. Qian BZ, Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141: 39-51.
20. Morikawa S, Baluk P, Kaidoh T, Haskell A, Jain RK, et al. (2002) Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol 160: 985-1000. (Pubitemid 34224587)
21. Ding Y, Song N, Luo Y (2012) Role of bone marrow-derived cells in angiogenesis: focus on macrophages and pericytes. Cancer Microenviron 5: 225-236.
22. Anfuso CD, Motta C, Giurdanella G, Arena V, Alberghina M, et al. (2014) Endothelial PKCα-MAPK/ERK-phospholipase A2 pathway activation as a response of glioma in a triple culture model. A new role for pericytes? Biochimie 99: 77-87.
23. Cheng L, Huang Z, Zhou W, Wu Q, Donnola S, et al. (2013) Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 153: 139-152.
24. Mravic M, Asatrian G, Soo C, Lugassy C, Barnhill RL, et al. (2014) From pericytes to perivascular tumours: correlation between pathology, stem cell biology, and tissue engineering. Int Orthop 02/2014. doi: 10.1007/s00264-014- 2295-0.
25. Rupp C, Scherzer M, Rudisch A, Unger C, Haslinger C, et al. (2014) IGFBP7, a novel tumor stroma marker, with growth-promoting effects in colon cancer through a paracrine tumor-stroma interaction. Oncogene 0. doi: 10.1038/onc.2014.18.
26. Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, et al. (2012) Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 151: 1542-1556.
27. Berger M, Bergers G, Arnold B, Hämmerling GJ, Ganss R (2005) Regulator of G-protein signaling-5 induction in pericytes coincides with active vessel remodeling during neovascularization. Blood 105: 1094-1101. (Pubitemid 40170880)
28. Hamzah J, Jugold M, Kiessling F, Rigby P, Manzur M, et al. (2008) Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature 453: 410-414. (Pubitemid 351693122)
29. Harris AK, Wild P, Stopak D (1980) Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208: 177-179. (Pubitemid 10072133)
30. Etienne-Manneville S (2004) Cdc42-the centre of polarity. J Cell Sci 117: 1291-1300.
31. Bourguignon LY (2008) Hyaluronan-mediated CD44 activation of RhoGTPase signaling and cytoskeleton function promotes tumor progression. Semin Cancer Biol 18: 251-259.
32. Yemisci M, Gursoy-Ozdemir Y, Vural A, Can A, Topalkara K, et al. (2009) Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat Med 15: 1031-1037.
33. Pelish HE, Peterson JR, Salvarezza SB, Rodriguez-Boulan E, Chen JL, et al. (2006) Secramine inhibits Cdc42-dependent functions in cells and Cdc42 activation in vitro. Nat Chem Biol 2: 39-46.
34. Cui W, Ke JZ, Zhang Q, Ke HZ, Chalouni C, et al. (2006) The intracellular domain of CD44 promotes the fusion of macrophages. Blood 107: 796-805. (Pubitemid 43076408)
35. Li N, Zhang J, Liang Y, Shao J, Peng F, et al. (2007) A controversial tumor marker: is SM22 a proper biomarker for gastric cancer cells? J Proteome Res 6: 3304-3312. (Pubitemid 47310214)
36. Armulik A, Genové G, Betsholtz C (2011) Pericytes: developmental, physiological and pathological perspectives, problems, and promises. Dev Cell 21: 193-215.
37. Venere M, Fine HA, Dirks PB, Rich JN (2011) Cancer stem cells in gliomas: identifying and understanding the apex cell in cancer's hierarchy. Glia 59: 1148-1154.
38. Fomchenko EI, Dougherty JD, Helmy KY, Katz AM, Pietras A, et al. (2011) Recruited cells can become transformed and overtake PDGF-induced murine gliomas in vivo during tumor progression. PLoS One 6: e20605. doi: 10.1371/journal.pone. 0020605.
39. Pàez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, et al. (2009) Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15: 220-231.
40. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: The next generation. Cell 144: 646-674.
41. Murphy DA, Courtneidge SA (2011) The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol 12: 413-426.
42. Oser M, Dovas A, Cox D, Condeelis J (2011) Nck1 and Grb2 localization patterns can distinguish invadopodia from podosomes. Eur J Cell Biol 90: 181-188.
43. Stylli SS, Kaye AH, Lock P (2008) Invadopodia: at the cutting edge of tumour invasion. J Clin Neurosci 15: 725-737.
44. Ridley AJ (2011) Life at the leading edge. Cell 145: 1012-1022.
45. Gunst SJ, Zhang W (2008) Actin cytoskeletal dynamics in smooth muscle: a new paradigm for the regulation of smooth muscle contraction. Am J Physiol Cell Physiol 295: C576-C587.
46. Gadea G, Sanz-Moreno V, Self A, Godi A, Marshall CJ (2008) DOCK10-mediated Cdc42 activation is necessary for amoeboid invasion of melanoma cells. Curr Biol 18: 1456-1465.
47. Yiin JJ, Hu B, Jarzynka MJ, Feng H, Liu KW, et al. (2009) Slit2 inhibits glioma cell invasion in the brain by suppression of Cdc42 activity. Neuro Oncol 11: 779-789.
48. Hirata E, Yukinaga H, Kamioka Y, Arakawa Y, Miyamoto S, et al. (2012) In vivo fluorescence resonance energy transfer imaging reveals differential activation of Rho-family GTPases in glioblastoma cell invasion. J Cell Sci 125: 858-868.
49. Gadéa G, Lapasset L, Gauthier-Rouvière C, Roux P (2002) Regulation of Cdc42-mediated morphological effects: a novel function for p53. EMBO J 21: 2373-2382. (Pubitemid 34546710)
50. Martin-Belmonte F, Gassama A, Datta A, Yu W, Rescher U, et al. (2007) PTEN-mediated segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128: 383-397. (Pubitemid 46123512)
51. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, et al. (2008) p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 455: 1129-1133.
52. Yemisci M, Gursoy-Ozdemir Y, Vural A, Can A, Topalkara K, et al. (2009) Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat Med 15: 1031-1037.
53. De Sanctis F, Sandri S, Ferrarini G, Pagliarello I, Sartoris S, et al. (2014) The emerging immunological role of post-translational modifications by reactive nitrogen species in cancer microenvironment. Front Immunol 5: 69. doi: 10.3389/fimmu.2014.00069.
54. Tang X (2013) Tumor-associated macrophages as potential diagnostic and prognostic biomarkers in breast cancer. Cancer Lett 332: 3-10.
55. Travaglione S, Falzano L, Fabbri A, Stringaro A, Fais S, et al. (2002) Epithelial cells and expression of the phagocytic marker CD68: scavenging of apoptotic bodies following Rho activation. Toxicol In Vitro 16: 405-411. (Pubitemid 34756431)
56. Ploeger DT, Hosper NA, Schipper M, Koerts JA, de Rond S, et al. (2013) Cell plasticity in wound healing: paracrine factors of M1/M2 polarized macrophages influence the phenotypical state of dermal fibroblasts. Cell Commun Signal 11: 29. doi: 10.1186/1478-811X-11-29.
57. Döme B, Timár J, Paku S (2003) A novel concept of glomeruloid body formation in experimental cerebral metastases. J Neuropathol Exp Neurol 62: 655-661. (Pubitemid 36682638)
58. Del Duca D, Werbowetski T, Del Maestro RF (2004) Spheroid preparation from hanging drops: characterization of a model of brain tumor invasion. J Neurooncol 67: 295-303. (Pubitemid 39137360)
59. Oishi K, Kamiyashiki T, Ito Y (2007) Isometric contraction of microvascular pericytes from mouse brain parenchyma. Microvasc Res 73: 20-28. (Pubitemid 46072895)
60. Xu B, Pelish H, Kirchhausen T, Hammond GB (2006) Large scale synthesis of the Cdc42 inhibitor secramine A and its inhibition of cell spreading. Org Biomol Chem 4: 4149-4157. (Pubitemid 44665187)
61. Hirase H, Creso J, Singleton M, Barthó P, Buzsáki G (2004) Two-photon imaging of brain pericytes in vivo using dextran-conjugated dyes. Glia 46: 95-100. (Pubitemid 38461726)
62. Zhu X, Bergles DE, Nishiyama A (2008) NG2 cells generate both oligodendrocytes and grey matter astrocytes. Development 135: 145-157. (Pubitemid 351201488)
63. Hinz B, Celetta G, Tomasek JJ, Gabbiani G, Chaponnier C (2001) Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 12: 2730-2741. (Pubitemid 33051938)
64. Pelegrin P, Surprenant A (2009) Dynamics of macrophage polarization reveal new mechanism to inhibit IL-1 βeta release through pyrophosphates. EMBO J 28: 2114-2127.
65. Goding JW (2000) Ecto-enzymes: physiology meets pathology. J Leukoc Biol 67: 285-311.
66. Atkinson B, Dwyer K, Enjyoji K, Robson SC (2006) Ecto-nucleotidases of the CD39/NTPDase family modulate platelet activation and thrombus formation: Potential as therapeutic targets. Blood Cells Mol Dis 36: 217-222.
67. Xu S, Shao QQ, Sun JT, Yang N, Xie Q, et al. (2013) Synergy between the ectoenzymes CD39 and CD73 contributes to adenosinergic immunosuppression in human malignant gliomas. Neuro Oncol 15: 1160-1172.
68. Bageritz J, Puccio L, Piro RM, Hovestadt V, Phillips E, et al. (2014) Stem cell characteristics in glioblastoma are maintained by the ecto-nucleotidase E-NPP1. Cell Death Differ 21: 929-940.
69. Allard B, Turcotte M, Stagg J (2012) CD73-generated adenosine: orchestrating the tumor-stroma interplay to promote cancer growth. J Biomed Biotechnol 2012: 485156. doi: 10.1155/2012/485156.
70. Pellegatti P, Falzoni S, Donvito G, Lemaire I, Di Virgilio F (2011) P2X7 receptor drives osteoclast fusion by increasing the extracellular adenosine concentration. FASEB J 25: 1264-1274.